Developmental age is a strong determinant of stress responses in plants. Differential susceptibility to various environmental stresses is widely observed at both the organ and whole-plant level. While it is clear that age determines stress susceptibility, the causes, regulatory mechanisms, and functions are only now beginning to emerge. Compared with concepts on age-related biotic stress resilience, advancements in the abiotic stress field are relatively limited. In this review, we focus on current knowledge of ontogenic resistance to abiotic stresses, highlighting examples at the organ (leaf) and plant level, preceded by an overview of the relevant concepts in plant aging. We also discuss age-related abiotic stress resilience mechanisms, speculate on their functional relevance, and outline outstanding questions. The Concept of AgingThe definitions of plant aging (see Glossary) are diverse. One might think of aging to comprehend the entire plant life cycle: from seed to senescence. However, this cycle is different for annuals and perennials. Annuals and biennials are semelparous (monocarpic) species that undergo their complete life cycle in one or two growing seasons, respectively. Perennials are iteroparous (polycarpic) species that live for many years with a clear disjunction between plant and organ lifespan. In this review, we mainly focus on age-related aspects of annuals, but some concepts are equivalent to specific organs of perennials that undergo repeated yearly cycles. HighlightsThe processes of aging, such as leaf development, senescence, and phase transitions from juvenile to adult plants, are genetically programmed and highly controlled by complex regulatory pathways.During aging, plants alter their organ morphology, sink-source balances, and chemical composition, including changes in redox status and hormone levels, which will collectively determine how abiotic stress signals are perceived and processed.
Plant and plant organ movements are the result of a complex integration of endogenous growth and developmental responses, partially controlled by the circadian clock, and external environmental cues. Monitoring of plant motion is typically done by image-based phenotyping techniques with the aid of computer vision algorithms. Here we present a method to measure leaf movements using a digital inertial measurement unit (IMU) sensor. The lightweight sensor is easily attachable to a leaf or plant organ and records angular traits in real-time for two dimensions (pitch and roll) with high resolution (measured sensor oscillations of 0.36° ± 0.53° for pitch and 0.50° ± 0.65° for roll). We were able to record simple movements such as petiole bending, as well as complex lamina motions, in several crops, ranging from tomato to banana. We also assessed growth responses in terms of lettuce rosette expansion and maize seedling stem movements. The IMU sensors are capable of detecting small changes of nutations (i.e., bending movements) in leaves of different ages and in different plant species. In addition, the sensor system can also monitor stress-induced leaf movements. We observed that unfavorable environmental conditions evoke certain leaf movements, such as drastic epinastic responses, as well as subtle fading of the amplitude of nutations. In summary, the presented digital sensor system enables continuous detection of a variety of leaf motions with high precision, and is a low-cost tool in the field of plant phenotyping, with potential applications in early stress detection.
Developing leaves undergo a vast array of age-related changes as they mature. These include physiological, hormonal and morphological changes that determine their adaptation plasticity towards adverse conditions. Waterlogging induces leaf epinasty in tomato, and the magnitude of leaf bending is intricately related to the age-dependent cellular and hormonal response. We now show that ethylene, the master regulator of epinasty, is differentially regulated throughout leaf development, giving rise to age-dependent epinastic responses. Young leaves have a higher basal ethylene production, but are less responsive to waterlogging-induced epinasty, as they have a higher capacity to convert the root-borne and mobilized ACC into the inactive conjugate MACC. Ethylene stimulates cell elongation relatively more at the adaxial petiole side, by activating auxin biosynthesis and locally inhibiting its transport through PIN4 and PIN9 in older and mature leaves. As a result, auxins accumulate in the petiole base of these leaves and enforce partially irreversible epinastic bending upon waterlogging. Young leaves maintain their potential to transport auxins, both locally and through the vascular tissue, leading to enhanced flexibility to dampen the epinastic response and a faster upwards repositioning during reoxygenation. This mechanism also explains the observed reduction of epinasty during and its recovery after waterlogging in the anthocyanin reduced (are) and Never ripe (Nr) mutants, both characterized by higher auxin flow. Our work has demonstrated that waterlogging activates intricate hormonal crosstalk between ethylene and auxin, controlled in an age-dependent way.
In tomato, downward leaf bending is a morphological adaptation towards waterlogging, which has been shown to induce a range of metabolic and hormonal changes. This kind of functional trait is often the result of a complex interplay of regulatory processes starting at the gene level, gated through a plethora of signaling cascades and modulated by environmental cues. Through phenotypical screening of a population of 54 tomato accessions in a Genome Wide Association Study (GWAS), we have identified target genes potentially involved in plant growth and survival during waterlogging and subsequent recovery. Changes in both plant growth rate and epinastic descriptors revealed several associations to genes possibly supporting metabolic activity in low oxygen conditions in the root zone. In addition to this general reprogramming, some of the targets were specifically associated to leaf angle dynamics, indicating these genes might play a role in the induction, maintenance or recovery of differential petiole elongation in tomato during waterlogging.
In tomato, downward leaf bending is a morphological adaptation towards waterlogging, which has been shown to induce a range of metabolic and hormonal changes. This kind of functional trait is often the result of a complex interplay of regulatory processes starting at the gene level, gated through a plethora of signaling cascades and modulated by environmental cues. Through phenotypical screening of a population of 54 tomato accessions in a Genome Wide Association Study (GWAS), we have identified target genes potentially involved in plant growth and survival during waterlogging and subsequent recovery. Changes in both plant growth rate and epinastic descriptors revealed several associations to genes possibly supporting metabolic activity in low oxygen conditions in the root zone. In addition to this general reprogramming, some of the targets were specifically associated to leaf angle dynamics, indicating these genes might play a role in the induction, maintenance or recovery of differential petiole elongation in tomato during waterlogging.
Waterlogging leads to hypoxic conditions in the root zone that subsequently cause systemic adaptive responses in the shoot, including leaf epinasty. Waterlogging-induced epinasty in tomato has long been ascribed to the coordinated action of ethylene and auxins. However, other hormonal signals have largely been neglected, despite evidence of their importance in leaf posture control. To adequately cover a large group of growth regulators, we performed a tissue-specific and time-dependent hormonomics analysis. This analysis revealed that multiple hormones are differentially affected throughout a 48 h waterlogging treatment, and, more importantly, that leaf development defines a framework in which this hormonal control is regulated. In addition, we could distinguish early hormonal signals that might contribute to fast responses towards oxygen deprivation from those that potentially sustain the waterlogging response. For example, abscisic acid (ABA) levels peak in petioles within the first 12 h of the treatment, while its metabolites only rise much later, suggesting ABA transport is altered. At the same time, cytokinins (CK) and their derivatives drastically decline during waterlogging in leaves of all ages. This drop in CK possibly releases the inhibition of ethylene and auxin mediated cell elongation to establish epinastic bending. Auxins themselves rise substantially in the petiole of mature leaves, but mostly after 48 h of root hypoxia. Based on our hormone profiling, we propose that ethylene and ABA might act synergistically to dynamically fine-tune the balance of IAA and CK in the petiole, ultimately leading to differential growth and epinasty during waterlogging.
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